Regulation and deregulation of E2F1 in postmitotic neurons differentiated from embryonal carcinoma P19 cells

Experimental Cell Research

Volumn 251, Issue 2, 1999, Pages 442-451

  Azuma Hara, Mizuki ^a   Taniura, Hideo ^a   Uetsuki, Taichi ^a   Niinobe, Michio ^a   Yoshikawa, Kazuaki ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

Adenovirus vector; Apoptosis; E2F1; Postmitotic neurons; Proteasome; Ubiquitination

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; BROXURIDINE; COMPLEMENTARY DNA; HYBRID PROTEIN; MESSENGER RNA; PROTEASOME; TRANSCRIPTION FACTOR E2F; UBIQUITIN;

ADENOVIRUS; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE S PHASE; CELL LYSATE; CHROMATIN CONDENSATION; CONTROLLED STUDY; ELECTROPHORETIC MOBILITY; EMBRYO; EMBRYONAL CARCINOMA; IN VITRO STUDY; MITOSIS; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; NORTHERN BLOTTING; PRIORITY JOURNAL; WESTERN BLOTTING;

ADENOVIRIDAE; ANIMALIA; MURINAE;

EID: 0033568318     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1006/excr.1999.4593     Document Type: Article

References (45)

1. Helin K., Lees J. A., Vidal M., Dyson N., Harlow E., Fattaey A. A cDNA encoding a pRB-binding protein with properties of the transcription factor E2F. Cell. 70:1992;337-350.
2. Kaelin W. G., Krek W., Sellers W. R., DeCaprio J. A., Ajchenbaum F., Fuchs C. S., Chittenden T., Li Y., Farnham P. J., Blanar M. A., Livingston D. M., Flemington E. K. Expression cloning of a cDNA encoding a retinoblastoma-binding protein with E2F-like properties. Cell. 70:1992;351-364.
3. Nevins J. R. E2F: A link between the Rb tumor suppressor protein and viral oncoproteins. Science. 258:1992;424-429.
4. Weinberg R. A. The retinoblastoma protein and cell cycle control. Cell. 81:1995;323-330.
5. Dupont E., Sansal I., Evrard C., Rouget P. Developmental pattern of expression of NPDC-1 and its interaction with E2F-1 suggest a role in the control of proliferation and differentiation of neural cells. J. Neurosci. Res. 51:1998;257-267.
6. Dagnino L., Fry C. J., Bartley S. M., Farnham P., Gallie B. L., Phillips R. A. Expression patterns of the E2F family of transcription factors during mouse nervous system development. Mech. Dev. 66:1997;13-25.
7. 3H-thymidine incorporation and neurogenesis. J. Neurosci. 13:1993;2930-2938.
8. Slack R. S., Hamel P. A., Bladon T. S., Gill R. M., McBurney M. W. Regulated expression of the retinoblastoma gene in differentiating embryonal carcinoma cells. Oncogene. 8:1993;1585-1591.
9. Maruyama K., Usami M., Aizawa T., Yoshikawa K. A novel brain-specific mRNA encoding nuclear protein (necdin) expressed in neurally differentiated embryonal carcinoma cells. Biochem. Biophys. Res. Commun. 178:1991;291-296.
10. Hayashi Y., Matsuyama K., Takagi K., Sugiura H., Yoshikawa K. Arrest of cell growth by necdin, a nuclear protein expressed in postmitotic neurons. Biochem. Biophys. Res. Commun. 213:1995;317-324.
11. Taniura H., Taniguchi N., Hara M., Yoshikawa K. Necdin, a postmitotic neuron-specific growth suppressor, interacts with viral transforming proteins and cellular transcription factor E2F1. J. Biol. Chem. 273:1998;720-728.
12. Hofmann F., Martelli F., Livingston D. M., Wang Z. The retinoblastoma gene product protects E2F-1 from degradation by the ubiquitin-proteasome pathway. Genes Dev. 10:1996;2949-2959.
13. Hateboer G., Kerkhoven R. M., Shvarts A., Bernards R., Beijersbergen R. L. Degradation of E2F by the ubiquitin-proteasome pathway: Regulation by retinoblastoma family proteins and adenovirus transforming proteins. Genes Dev. 10:1996;2960-2970.
14. Campanero M. R., Flemington E. K. Regulation of E2F through ubiquitin-proteasome-dependent degradation: Stabilization by the pRB tumor suppressor protein. Proc. Natl. Acad. Sci. USA. 94:1997;2221-2226.
15. McBurney M. W., Jones-Villeneuve E. M., Edwards M. K., Anderson P. J. Control of muscle and neuronal differentiation in a cultured embryonal carcinoma cell line. Nature. 299:1982;165-167.
16. McBurney M. W., Reuhl K. R., Ally A. I., Nasipuri S., Bell J. C., Craig J. Differentiation and maturation of embryonal carcinoma-derived neurons in cell culture. J. Neurosci. 8:1988;1063-1073.
17. Slack R. S., Skerjanc I. S., Lach B., Craig J., Jardine K., McBurney M. W. Cells differentiating into neuroectoderm undergo apoptosis in the absence of functional retinoblastoma family proteins. J. Cell Biol. 129:1995;779-788.
18. Gill R. M., Slack R., Kiess M., Hamel P. A. Regulation of expression and activity of distinct pRB, E2F, D-type cyclin, and CKI family members during terminal differentiation of P19 cells. Exp. Cell Res. 244:1998;157-170.
19. Reichel R. R. Regulation of E2F/cyclin A-containing complex upon retinoic acid-induced differentiation of teratocarcinoma cells. Gene Expr. 2:1992;259-271.
20. Corbeil H. B., Whyte P., Branton P. E. Characterization of transcription factor E2F complexes during muscle and neuronal differentiation. Oncogene. 11:1995;909-920.
21. Jones-Villeneuve E. M., McBurney M. W., Rogers K. A., Kalnins V. I. Retinoic acid induces embryonal carcinoma cells to differentiate into neurons and glial cells. J. Cell Biol. 94:1982;253-262.
22. Rudnicki M. A., McBurney M. W. Cell culture methods and induction of differentiation of embryonal carcinoma cell lines. Robertoson E. J. Teratocarcinomas and Embryonic Stem Cells: A Practical Approach. 1987;IRL Press, Oxford.
23. Uetsuki T., Takagi K., Sugiura H., Yoshikawa K. Structure and expression of the mouse necdin gene. Identification of a postmitotic neuron-restrictive core promoter. J. Biol. Chem. 271:1996;918-924.
24. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:1987;156-159.
25. Yoshikawa K., Williams C., Sabol S. L. Rat brain preproenkephalin mRNA. cDNA cloning, primary structure, and distribution in the central nervous system. J. Biol. Chem. 259:1984;14301-14308.
26. Helin K., Harlow E. Heterodimerization of the transcription factors E2F-1 and DP-1 is required for binding to the adenovirus E4 (ORF6/7) protein. J. Virol. 68:1994;5027-5035.
27. Lukas J., Petersen B. O., Holm K., Bartek J., Helin K. Deregulated expression of E2F family members induces S-phase entry and overcomes p16INK4A-mediated growth suppression. Mol. Cell. Biol. 16:1996;1047-1057.
28. Mullen R. J., Buck C. R., Smith A. M. NeuN, a neuronal specific nuclear protein in vertebrates. Development. 116:1992;201-211.
29. Schreiber E., Matthias P., Muller M. M., Schaffner W. Rapid detection of octamer binding proteins with 'mini-extracts,' prepared from a small number of cells. Nucleic Acids Res. 17:1989;6419.
30. Schwarz J. K., Bassing C. H., Kovesdi I., Datto M. B., Blazing M., George S., Wang X. F., Nevins J. R. Expression of the E2F1 transcription factor overcomes type beta transforming growth factor-mediated growth suppression. Proc. Natl. Acad. Sci. USA. 92:1995;483-487.
31. Nishimura I., Uetsuki T., Dani S. U., Ohsawa Y., Saito I., Okamura H., Uchiyama Y., Yoshikawa K. Degeneration in vivo of rat hippocampal neurons by wild-type Alzheimer amyloid precursor protein overexpressed by adenovirus-mediated gene transfer. J. Neurosci. 18:1998;2387-2398.
32. Jensen T. J., Loo M. A., Pind S., Williams D. B., Goldberg A. L., Riordan J. R. Multiple proteolytic systems, including the proteasome, contribute to CFTR processing. Cell. 83:1995;129-135.
33. Aizawa T., Haga S., Yoshikawa K. Neural differentiation-associated generation of microglia-like phagocytes in murine embryonal carcinoma cell line. Dev. Brain Res. 59:1991;89-97.
34. Qin X. Q., Livingston D. M., Kaelin W. G. Jr., Adams P. D. Deregulated transcription factor E2F-1 expression leads to S-phase entry and p53-mediated apoptosis. Proc. Natl. Acad. Sci. USA. 91:1994;10918-10922.
35. Kowalik T. F., DeGregori J., Schwarz J. K., Nevins J. R. E2F1 overexpression in quiescent fibroblasts leads to induction of cellular DNA synthesis and apoptosis. J. Virol. 69:1995;2491-2500.
36. Lee E. Y.-H. P., Chang C.-Y., Hu N., Wang Y.-C. J., Lai C.-C., Herrup K., Lee W.-H., Bradley A. Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis. Nature. 359:1992;288-294.
37. Jacks T., Fazeli A., Schmitt E. M., Bronson R. T., Goodell M. A., Weinberg R. A. Effects of an Rb mutation in the mouse. Nature. 359:1992;295-300.
38. Clarke A. R., Maandag E. R., van Roon M., van der Lugt N. M., van der Valk M., Hooper M. L., Berns A., te Riele H. Requirement for a functional Rb-1 gene in murine development. Nature. 359:1992;328-330.
39. Lee E. Y., Hu N., Yuan S. S., Cox L. A., Bradley A., Lee W. H., Herrup K. Dual roles of the retinoblastoma protein in cell cycle regulation and neuron differentiation. Genes Dev. 8:1994;2008-2021.
40. Du W., Xie J. E., Dyson N. Ectopic expression of dE2F and dDP induces cell proliferation and death in the Drosophila eye. EMBO J. 15:1996;3684-3692.
41. Suda K., Holmberg E. G., Nornes H. O., Neuman T. DNA synthesis is induced in adult neurons after expression of E2F1 and E1A. Neuroreport. 5:1994;1749-1751.
42. Hsieh J. K., Fredersdorf S., Kouzarides T., Martin K., Lu X. E2F1-induced apoptosis requires DNA binding but not transactivation and is inhibited by the retinoblastoma protein through direct interaction. Genes Dev. 11:1997;1840-1852.
43. Phillips A. C., Bates S., Ryan K. M., Helin K., Vousden K. H. Induction of DNA synthesis and apoptosis are separable functions of E2F-1. Genes Dev. 11:1997;1853-1863.
44. Schmidt-Kastner P. K., Jardine K., Cormier M., McBurney M. W. Absence of p53-dependent cell cycle regulation in pluripotent mouse cell lines. Oncogene. 16:1998;3003-3011.
45. Blaschke A. J., Staley K., Chun J. Widespread programmed cell death in proliferative and postmitotic regions of the fetal cerebral cortex. Development. 122:1996;1165-1174.